1.1 A brief history
The coolness of peppermint, the warmth of cinnamon, the heat of chilis, the tingling of carbonated beverages, the sting from a bee, the itch from a mosquito bite, the pungency of sniffed ammonia, the pain from an inflamed joint ā these diverse sensations all share a common basis in chemesthesis. Not limited to the nose and mouth but experienced throughout much of the body, chemesthesis might simply be described as the chemical sensitivity of the body that is not served by the senses of taste or smell. But such a definition would not convey either the neurobiological complexity or the varied and important functions of chemesthesis. These and the concept of chemesthesis can be better appreciated by first considering the venerable concept that it replaced: āthe common chemical senseā.
For much of the 20th century, researchers in the chemical senses and related fields considered the common chemical sense to be a third specialized chemosense in addition to taste and smell. The concept was proposed by the Harvard zoologist G.H. Parker (1912) to describe the chemical sensitivity of the integument of fish and amphibians, which had previously simply been referred to as āthe chemical senseā or āthe undifferentiated chemical senseā. By cutting individual cranial nerves and observing behavioral responses to concentrated solutions of HCl, NaOH, NaCl, and quinine applied to the bodies and tails of two species of fish, Parker concluded the sensitivity to chemical irritants was a property of āordinary spinal nervesā rather than of the gustatory and olfactory nerves. He further proposed that the common chemical sense was a sensory system in vertebrates āas distinct as smell or tasteā (Parker, 1912, p. 221), though closer in sensitivity and function to taste than to smell. A few years later, Crozier (1916) performed experiments on frogs that he argued provided further support for a common chemical sense. Some decades later, in his book titled The Chemical Senses, Moncrieff (1944) lent further credence to the concept by describing the common chemical sense as a separate modality that functions in concert with taste and smell.
However, some researchers were unhappy with the concept and argued instead that the chemical sensitivity of the skin and mucus membranes was a property of the sense of pain. Among them was M.H. Jones (1954), who conducted a study of her own after complaining that āthe ācommon chemical senseā is accepted by some writers without much tangible evidence and summarily rejected by others without much better evidenceā (Jones, 1954, p. 696). Jones found that application of cocaine to the mucosal surface of the lower lip in humans reduced sensitivity to mechanical pain as well as to chemical pain, and so concluded that both forms of stimulation were sensed by cutaneous nerve endings of the pain system. In support of this conclusion, Jones quoted from Carl Pfaffmannās (1951) chapter on the chemical senses in Stevensā Handbook of Experimental Psychology in which he wrote, āPain and the common chemical sensitivity appearā¦to be mediated by the same nerve endingsā (Pfaffmann, 1951, p. 1144). It is notable, however, that this quotation was taken from a section in the chapter with the heading āThe Common Chemical Senseā, in which Pfaffmann went on to say, āOn the other hand, it is quite clear that such chemical sensitivity is distinct from touch, and in the mouth and nose, distinct from taste and smellā (p. 1145). Pfaffmannās use of the term and affirmation of a chemical sensitivity separate from taste and smell may have helped to sustain the concept of a common chemical sense despite the clear evidence of its relationship to pain.
Further sustaining the terminology (if not Parkerās original concept) were papers by Keele and others (Armstrong et al., 1953; Bleehen and Keele, 1977; Keele, 1962) on the chemical sensitivity of pain, in which the possibility of specific āchemo-nociceptorsā was proposed. While this body of work demonstrated beyond a doubt that chemosensory irritation was mediated at least in part by receptors of the pain sense, it also implied that the common chemical sense was in fact a specialized chemical sensitivity within the pain sense. Indeed, Keele titled his 1962 paper āThe common chemical sense and its receptorsā. Other work published around the same time on the neurophysiological and perceptual response to capsaicin, the spicy-hot constituent of chilis (Jancso et al., 1968; Szolcsanyi, 1977; Szolcsanyi et al., 1988; Szolcsanyi and Jancso-Gabor, 1973), further strengthened the connection between pain and chemical irritation by showing that sensitization or desensitization by capsaicin also affected the sensitivity to both mechanical pain and heat pain (Green, 1986; Szolcsanyi, 1977; Szolcsanyi, 1985; Szolcsanyi et al., 1988). This work paralleled and supported Jonesā earlier evidence that cocaine reduced the sensitivity to both mechanical and chemical pain. Thus, whether or not specialized chemonociceptors existed, the evidence was clear that chemical irritants also stimulate nonspecific (polymodal) nociceptors, and thus are not sensed exclusively by a chemosensitive sub-modality of pain.
At about the same time the chemical sensitivity of the temperature senses was being brought to light through studies which showed that menthol evokes its sensory cooling effect by direct stimulation of cold fibers and not merely by evaporative cooling (Green, 1985; Schafer et al., 1986; Schafer et al., 1989). Remarkably, the sensitivity of cold fibers to menthol had been demonstrated decades before in electrophysiological studies of the gustatory nerves (Dodt et al., 1953; Hensel and Zotterman, 1951), but the earlier findings had not found their way into published discussions of the common chemical sense. Evidence that warm fibers could also be chemically stimulated was less clear (Foster and Ramage, 1981), although experiments showing that capsaicin-sensitive receptors played a role in thermoregulation, and that capsaicin increased the perceived temperature of warm or hot water sipped into the mouth, suggested that capsaicin could modulate the excitability of the warmth system (Green, 1986; Szolcsanyi and Jancso-Gabor, 1973).
It was at this stage of understanding that a symposium on āchemical irritationā was held at the Monell Chemical Senses Center in 1988. The symposium brought together leading researchers in diverse fields of study to present their latest findings and to discuss current understanding and future research directions. Dissatisfaction with the concept of the common chemical sense surfaced throughout the symposium and was a central topic in the closing discussion, but no agreement was reached on an alternative terminology. Not until the procee...
